Abstract

Profound knowledge of demographic history is a prerequisite for the understanding and inference of processes involved in the evolution of population differentiation and speciation. Together with new coalescent-based methods, the recent availability of genome-wide data enables investigation of differentiation and divergence processes at unprecedented depth. We combined two powerful approaches, full Approximate Bayesian Computation analysis (ABC) and pairwise sequentially Markovian coalescent modeling (PSMC), to reconstruct the demographic history of the split between two avian speciation model species, the pied flycatcher and collared flycatcher. Using whole-genome re-sequencing data from 20 individuals, we investigated 15 demographic models including different levels and patterns of gene flow, and changes in effective population size over time. ABC provided high support for recent (mode 0.3 my, range <0.7 my) species divergence, declines in effective population size of both species since their initial divergence, and unidirectional recent gene flow from pied flycatcher into collared flycatcher. The estimated divergence time and population size changes, supported by PSMC results, suggest that the ancestral species persisted through one of the glacial periods of middle Pleistocene and then split into two large populations that first increased in size before going through severe bottlenecks and expanding into their current ranges. Secondary contact appears to have been established after the last glacial maximum. The severity of the bottlenecks at the last glacial maximum is indicated by the discrepancy between current effective population sizes (20,000-80,000) and census sizes (5-50 million birds) of the two species. The recent divergence time challenges the supposition that avian speciation is a relatively slow process with extended times for intrinsic postzygotic reproductive barriers to evolve. Our study emphasizes the importance of using genome-wide data to unravel tangled demographic histories. Moreover, it constitutes one of the first examples of the inference of divergence history from genome-wide data in non-model species.

The term ‘relative size’ refers to the ratio of post-split effective population size and current effective population size (e.g. NPScoll/Ncoll). Population migration rate equals to 4N0mij, where N0 = 10,000.

The term ‘relative size’ refers to the ratio of post-split effective population size and current effective population size (e.g. NPScoll/Ncoll). Population migration rate equals to 4N0mij, where N0 = 10,000. Due to smoothing step of the parameter distributions the densities at the prior limits are underestimated.

PSMC estimate of the effective population size change over time for collared flycatcher.

The black curve is the PSMC estimate for the original data and the grey curves indicate PSMC estimates for 100 bootstrapped sequences. Glacial and interglacial periods of the Late and Middle Pleistocene are indicated by blue and yellow bars, respectively. The interglacial periods corresponds to Marine Isotope Stages: 5e, 7, 9, 11, 13, 15, and 17. The large red-shaded area corresponds to 50% HPDI of the time of divergence (RMASC model). LGP – last glacial period.